Plant Soil (2006) 284:1–5 DOI 10.1007/s11104-006-0047-7
COMMENTARY
Partitioning the components of soil respiration: a research challenge E. M. Baggs
Received: 18 January 2006 / Accepted: 23 February 2006 Ó Springer Science+Business Media B.V. 2006
Abstract Little is known about the respiratory components of CO2 emitted from soils and attaining a reliable quantification of the contribution of root respiration remains one of the major challenges facing ecosystem research. Resolving this would provide major advances in our ability to predict ecosystem responses to climate change. The merits and technical and theoretical difficulties associated with different approaches adopted for partitioning respiration components are discussed here. The way forward is suggested to be the development of non-invasive regression analysis validated by stable isotope approaches to increase the sensitivity of model functions to include components of rhizosphere microbial activity, changing root biomass and the dynamics of a wide range of soil C pools. Keywords CO2 flux Æ CO2 partitioning Æ Heterotrophic respiration Æ Root respiration Æ Soil respiration
Section Editor: A. Hodge. E. M. Baggs (&) School of Biological Sciences (Plant and Soil Science), University of Aberdeen, Cruickshank Building, St Machar Drive, AB24 3UU, Aberdeen, UK e-mail:
[email protected]
Why partition soil respiration? The global CO2 flux from soils is estimated to be within the range of 64–72 Gt C y)1, accounting for 20–38% of annual input of CO2–C to the atmosphere from terrestrial and marine sources (Raich and Schlesinger 1992), and is therefore an important regulator of climate change as well as determinant of net ecosystem C balance. Despite recent advances in analytical techniques, still little is known about the respiratory components comprising this emission, mainly due to problems in separating root (usually root and rhizosphere) respiration, generally referred to as autotrophic, from that of heterotrophic microorganisms utilising pre-formed C compounds. Although root respiration is thought to significantly contribute to net CO2 fluxes from soils (e.g. Cisneros-Dozal et al. 2006; Epron et al. 1999; Hendricks et al. 1993; Ho¨gberg et al. 2001; Raich and Schlesinger 1992), reliable and reproducible quantification of this contribution remains elusive, and is one of the major challenges facing ecosystems research. It is important to resolve this as root associated (autotrophic) and bulk soil respiration have been shown to respond differently to increasing temperature, exhibiting different Q10 values (Boone et al. 1998; Rey et al. 2002), thereby possibly altering the net C flux from soils, and the potential for C sequestration, providing important feedbacks for climate change (Davidson et al. 2000; Melillo et al. 2002). Increases in root and rhizosphere respiration may reflect increased C inputs to the soil
123
2
through photosynthesis (Ho¨gberg et al. 2001), specific root activity, or root biomass (Gregory 2006), whereas increased heterotrophic respiration may reduce the potential for C storage in the soil (Grace 2004). Thus quantifying the components of net soil respiration is vital for the prediction of ecosystem response to climate change, and for understanding the nature and extent of feedbacks between climate change and soil processes, and it is essential that the components of soil respiration are entered into climate change models separately. The contribution of root respiration has been estimated to be anywhere between 10 and 90% of the total net CO2 flux (Hanson et al. 2000). Bond-Lamberty et al. (2004) in part attribute this large variability to technical and theoretical problems associated with the different methods adopted for partitioning the respiration components, although it is difficult to say to what extent this masks underlying variability within or between ecosystems. Rodeghiero and Cescatti (2006, this issue) adopt an indirect approach to partitioning, using regression analysis to show that autotrophic respiration accounted for between 16 and 58% of total CO2 emission in seven evergreen forest ecosystems, with a lower contribution estimated with comparatively higher soil N availability. The advantage of such an approach is that it is non-invasive, and in that sense overcomes the main problem associated with methodologies for direct determination. To fully assess its merits and limitations it should, however, be considered in light of other conventional direct approaches.
Direct determination of root respiration These are traditionally subdivided into component integration, root exclusion and isotope labelling techniques and are reviewed in detail by Hanson et al. (2000) and Kuzyakov and Larionova (2005). Each of these involves disturbing the root–soil system to some extent, which in itself raises uncertainties as to the validity of results. In component integration CO2 emission is determined from different soil fractions, and their respective masses multiplied to give a total CO2 flux. The component emissions are usually considered validated if the additive emission is the same as that measured in situ, and heterotrophic activity is sometimes estimated by difference
123
Plant Soil (2006) 284:1–5
between the total CO2 flux, and root and litter components (e.g. Edwards and Harris 1977). A major problem with this approach is that root respiration rates are only measured in vitro, and removal and separation of soil components represents significant soil disturbance particularly of the root–soil interface, altering the soil atmosphere, and often separating roots from most of their associated microbial community (Trumbore 2006). A further development of the component integration method is a modification of the substrate-induced respiration approach of Anderson and Domsch (1978) to estimate autotrophic and heterotrophic respiration. The contribution of heterotrophic respiration is assumed to increase after addition of glucose to soil, but the autotrophic respiration assumed to remain unaltered (Ekblad and Ho¨gberg 2000). However, as with the component integration method, this approach involves disturbance of the soil system, and changes in the proportional contributions of the respiration components, particularly that of autotrophic respiration, when glucose is added in solution and roots are wetted (Kuzyakov and Larionova 2005). The main problem associated with root exclusion methodologies for determining respiration in the presence and absence of roots, is that soil disturbance increases CO2 emission, which either needs to be taken account of, or measurements delayed until after the system has returned to equilibrium (Bowden et al. 1993; Edwards 1991). Root removal experiments involve soil being placed back in situ after root removal, and further root growth prevented by barriers (e.g. Thierron and Laudelout 1996), whereas in trenching experiments existing roots are severed, but not removed, and a barrier is installed to inhibit future root growth (Boone et al. 1998; Bowden et al. 1993). However, soil water content tends to be greater after root severance or removal, affecting decomposition and respiration rates and microbial C and N pools (Hanson et al. 2000; Kuzyakov and Larionova 2005) and soil temperature can also be increased following the vegetation removal associated with clear cutting (Blet-Charaudeau et al. 1990; Brumme 1995). An increase in dead roots for heterotrophic decomposition occurs after clear cutting, along with removal of the continuous input of root exudates and other labile C compounds to soil. Arguably the most accurate, but certainly the most expensive, technique for partitioning the components
Plant Soil (2006) 284:1–5
of respiration is that of isotopic (14C or 13C) labelling. This typically takes the form of pulse (single or repeated) (e.g. Cheng et al. 1993; Gorissen et al. 1996; Rouhier et al. 1996) or continuous labelling (e.g. Liljeroth et al. 1994) through the plant, allowing in situ partitioning between root and soil respiration without the need for disturbance. 14C-labelling experiments have shown that an average of 14% of photosynthetically fixed C in perennial plants is lost as root respiration (Nguyen 2003). Short-term pulse labelling through the plant is advantageous because it reduces soil–plant disturbance, costs and experimental complexity, but it may poorly represent the range of C pools of interest as labile C compounds in the plant are preferentially labelled (Kuhns and Gjerstad 1991; Meharg and Killham 1988). Typically the labelled C within the plant is determined, and the root respiration estimated from the difference between that assimilated and that present in the biomass and soil at the time of measurement (Meharg and Killham 1988; Swinnen et al. 1994). The time period between label application and measurement is critical (Paterson et al. 1997) and preferential labelling of labile plant C compounds may result in an overestimate of root respiration of labelled C (Meharg and Killham 1988). Due to changes in plant C allocation over the growing season (Gregory and Atwell 1991), repeated pulse labelling is required to estimate the contribution of root respiration to annual CO2 fluxes from soil. The labelling of soil organic matter itself to partition respiration is contentious, as organic compounds, such as 14C-labelled glucose, may be subject to resorption by roots (Jones and Darrah 1992) meaning that measured 14C-CO2 may be derived from root as well as soil respiration. Continuous labelling, or application of the label over time periods comparable to that of the plant, may provide a more homogenous labelling of plant C pools. However, this has been criticised because it is not well suited to studying transient plant C dynamics, the equipment for this labelling is expensive for field studies, and over time the organic matter isotopic signature will be similar to that of the labelled plants, making a distinction between root respiration and soil respiration increasingly impossible (Meharg 1994). Alternative methods have been used, such as differentiating between the respiration of C4 plants from that of decomposition of C3-derived soil organic matter (Robinson and Scrimgeour 1995; Rochette and
3
Flanagan 1997), or C4- organic compounds from that of C3-plant-derived C (Ekblad and Ho¨gberg 2000), or applying CO2 at elevated concentrations (Andrews et al. 1999; Rouhier et al. 1996). Natural abundance 13 C signatures have been used to differentiate between sources of respiration (Dawson et al. 2002) as C respired by plants tends to be enriched in 13C, but heterotrophically derived CO2 is depleted in 13C, depending on fractionation processes (Trumbore 2006). However, as 13C signatures can change rapidly, a quantification of respiration components in unlikely with this approach. The tracing of ‘‘bomb’’ 14C has also recently been used to estimate autotrophic and heterotrophic sources of soil respiration (Borken et al. 2006; Trumbore et al. 2006).
Indirect determination of root respiration by regression analysis The regression analysis technique for partitioning soil CO2 fluxes is non-invasive, and can give an approximate quantification of root respiration to total soil respiration. Heterotrophic respiration is estimated from the y-intercept of the linear regression between surface CO2 fluxes and root biomass i.e. in the absence of roots. With this approach heterotrophic respiration is traditionally assumed, for simplification, to be spatially homogenous (Xu et al. 2001). What is most interesting about the results presented by Rodeghiero and Cescatti (2006) is that they provide a significant step forward in the development of this analysis by accounting for spatial heterogeneity and temporal variations in heterotrophic respiration in soil. This is likely to be significant due to heterogeneity of soil C, especially in the forest systems which the authors used to validate their approach, and because soil respiration varies spatially depending on C substrate proximity, seasonally and in response to plant phenology and root growth. They express the CO2 flux as the sum of the autotrophic and heterotrophic respiration, being linearly dependent on density of roots of 2–5 mm diameter, and soil C content to a depth of 30 cm. Different soil temperatures on different sampling dates facilitated investigation of the thermal and temporal dependencies of autotrophic and heterotrophic respiration. This is the first time that temporal variation in root respiration has been considered in such indirect analytical separation of
123
4
CO2 flux components and opens up opportunities for modelling soil respiration processes. As with any model serving to simplify a system this approach has its limitations. The separation method employed by Rodeghiero and Cescatti (2006) appears to be only suitable for sites where there is sufficient heterogeneity in both root density and soil C, and different coefficients of regression will need to be established when taking this methodology to different sites. The authors made no attempt to quantify changes in the fine root biomass to validate their model, but assumed, based on reports of Gill & Jackson (2000), that this biomass did not change over the year and therefore that this source of error would be negligible.
The way forward Partitioning of CO2 emission into root and soil respiration, by its very nature, oversimplifies the sources of CO2 emitted from soil. Root respiration is typically taken as a combination of all processes occurring in the rhizosphere, encompassing live-root respiration, mycorrhizal respiration and the activity of microorganisms utilising labile C derived from plant roots, and therefore includes a heterotrophic component. The boundary between autotrophic and heterotrophic respiration becomes even more blurred when considering mycorrhizal fungi obtaining C via symbiosis with plants, with uncertainties as to where the autotrophic respiration ends and the heterotrophic respiration begins. Differentiation of these rhizosphere components to attribute true autotrophic and heterotrophic contributions is a further challenge for ecosystem research, but can now be realised utilising recent developments in stable isotope techniques, such as stable isotope probing of nucleic acids (e.g. Rangel-Castro et al. 2005). Whilst regression analysis certainly has its place in the further development of techniques for partitioning soil respiration, advances in such indirect non-invasive estimates need to be validated by the most accurate direct approaches possible, such a stable isotope techniques. The challenge now for indirect approaches is to increase the sensitivity of the model functions to include the influence of rhizosphere microbial activity and community structure on these fluxes, effects of changing environmental conditions, and changes
123
Plant Soil (2006) 284:1–5
in root biomass and C input over time. There is also need to encompass the dynamics of the whole range of soil C pools, including slow C turnover in soil, which is more likely to be important in C sequestration. Acknowledgement The author’s work is supported by an Advanced Research Fellowship awarded by the Natural Environment Research Council (NERC), U.K.
References Anderson JPE, Domsch KH (1978) A physiological method for the quantitative measurement of microbial biomass in soils. Soil Biol Biochem 10:215–221 Andrews JA, Harrison KG, Matamala R, Schlesinger WH (1999) Separation of root respiration from total soil respiration using carbon-13 labelling during Free-Air Carbon dioxide Enrichment (FACE). Soil Sci Soc Am J 63:1429– 1435 Blet-Charaudeau C, Muller J, Laudelout H (1990) Kinetics of carbon dioxide evolution in relation to microbial biomass and temperature. Soil Sci Soc Am J 54:1324–1328 Bond-Lamberty B, Wang C, Gower ST (2004) A global relationship between the heterotrophic and autotrophic components of soil respiration? Global Change Biol 10:1756–1766 Boone RD, Nadelhoffer KJ, Canary JD, Kaye JP (1998) Roots exert a strong influence on the temperature sensitivity of soil respiration. Nature 396:570–572 Borken W, Savage K, Davidson EA, Trumbore SE (2006) Effects of experimental drought on soil respiration and radiocarbon efflux from a temperate forest soil. Global Change Biol 12:177–193 Bowden RD, Nadelhoffer KJ, Boone RD, Melillo JM, Garrison JB (1993) Contributions of above ground litter, below ground litter, and root respiration to total soil respiration in a temperate mixed hardwood forest. Can J For Res 23:1402–1407 Brumme R (1995) Mechanisms of carbon and nutrient release and retention in beech forest gaps. Plant Soil 169:593–600 Cheng W, Coleman DC, Carroll R, Hoffman CA (1993) In situ measurement of root respiration and soluble C concentrations in the rhizosphere. Soil Biol Biochem 25:1189–1196 Cisneros-Dozal LM, Trumbore S, Hanson PJ (2006) Partitioning sources of soil-respired CO2 and their seasonal variation using a unique radiocarbon tracer. Global Change Biol 12:194–204 Davidson EA, Trumbore SE, Amundson R (2000) Soil warming and carbon content. Nature 408:789–790 Dawson TE, Mambelli S, Plamboeck AH, Templer PH, Tu KP (2002) Stable isotopes in plant ecology. Ann Rev Ecol Syst 33:507–559 Edwards NT (1991) Root and soil respiration responses to ozone in Pinus taeda L. seedlings. New Phytol 118:315–321
Plant Soil (2006) 284:1–5 Edwards NT, Harris WF (1977) Carbon cycling in a mixed deciduous forest floor. Ecology 58:431–437 Ekblad A, Ho¨gberg P (2000) Analysis of d13C of CO2 distinguishes between microbial respiration of added C4-sucrose and other soil respiration in a C3-ecosystem. Plant Soil 219:197–209 Epron D, Farque L, Lucot E, Badot PM (1999) Soil CO2 efflux in a beech forest: the contribution of root respiration. Ann Forest Sci 56:289–295 Gill RA, Jackson RB (2000) Global patterns of root turnover for terrestrial ecosystems. New Phytol 147:13–31 Gorissen A, Kuikman PJ, Van Ginkel JH, Van De Beek H, Jansen AG (1996) ESPAS – an advanced phytotron for measuring carbon dynamics in a whole plant–soil system. Plant Soil 179:81–87 Grace J (2004) Understanding and managing the global carbon cycle. J Ecol 92:189–202 Gregory PJ (2006) Roots, rhizosphere and soil: the route to a better understanding of soil science. Eur J Soil Sci 57:2–12 Gregory PJ, Atwell BJ (1991) The fate of carbon in pulselabelled crops of barley and wheat. Plant Soil 136:205–213 Hanson PJ, Edwards NT, Garten CT, Andrews JA (2000) Separating root and soil microbial contributions to soil respiration: a review of methods and observations. Biogeochemistry 48:115–146 Hendricks JJ, Nadelhoffer KJ, Aber JD (1993) Assessing the role of fine roots in carbon and nutrient cycling. Trends Ecol Evol 8:174–178 Ho¨gberg P, Nordgren A, Buchmann N, Taylor AFS, Ekblad A, Hogberg MN, Nyberg G, Ottosson-Lofvenius M, Read DJ (2001) Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature 411:789–792 Jones DL, Darrah PR (1992) Re-sorption of organic components by roots of Zea mays L. and its consequences in the rhizosphere. Plant Soil 143:259–266 Kuhns MR, Gjerstad DH (1991) Distribution of 14C-labeled photosynthate in loblolly pine (Pinus taeda) seedlings as affected by season and time of exposure. Tree Physiol 8:259–271 Kuzyakov Y, Larionova AA (2005) Root and rhizomicrobial respiration: a review of approaches to estimate respiration by autotrophic and heterotrophic organisms in soil. J Plant Nutr Soil Sci 168:503–520 Liljeroth E, Kuikman P, Van Veen JA (1994) Carbon translocation to the rhizosphere of maize and wheat and influence on the turnover of native soil organic matter at different soil nitrogen levels. Plant Soil 161:233–240 Meharg AA (1994) A critical review of labelling techniques used to quantify rhizosphere carbon flow. Plant Soil 166:55–62 Meharg AA, Killham K (1988) A comparison of carbon flow from pre-labelled and pulse- labelled plants. Plant Soil 112:225–231
5 Melillo JM, Steudler PA, Aber JD, Newkirk K, Lux H, Bowles FP, Catricala C, Magill A, Ahrens T, Morrisseau S (2002) Soil warming and carbon cycle feedbacks to the climate system. Science 298:2173–2176 Nguyen C (2003) Rhizodeposition of organic C by plants: mechanisms and controls. Agronomie 23:375–396 Paterson E, Hall JM, Rattray EAS, Griffiths BS, Ritz K, Killham K (1997) Effect of elevated CO2 on rhizospere carbon flow and soil microbial processes. Global Change Biol 3:363–377 Raich JW, Schlesinger WH (1992) The global carbon dioxide flux in soil respiration and its relationship to vegetation and climate. Tellus 44B:81–99 Rangel-Castro JI, Killham K, Ostle N, Nicol GW, Anderson IC, Scrimgeour CM, Ineson P, Meharg A, Prosser JI (2005) Stable isotope probing analysis of the influence of liming on root exudate utilization by soil microorganisms. Environ Microbiol 7:828–838 Rey A, Pegoraro E, Tedeschi V, de Parri I, Jarvis PG, Valentini R (2002) Annual variation in soil respiration and its components in a coppice oak forest in Central Italy. Global Change Biol 8:851–866 Robinson D, Scrimgeour CM (1995) The contribution of plant C to soil CO2 measured using d13C. Soil Biol Biochem 27:1653–1656 Rochette P, Flanagan LB (1997) Quantifying rhizosphere respiration in a corn crop under field conditions. Soil Sci Soc Am J 61:466–474 Rodeghiero M, Cescatti A (2006) Indirect partitioning of soil respiration in a series of evergreen forest ecosystems. Plant Soil (this issue) Rouhier H, Billes G, Billes L, Bottner P (1996) Carbon fluxes in the rhizosphere of sweet chestnut seedlings (Castanea sativa) grown under two atmospheric CO2 concentrations: C-14 partitioning after pulse labelling. Plant Soil 180:101–111 Swinnen J, Van Veen JA, Merckx R (1994) 14C pulse-labelling of field-grown spring wheat: an evaluation of its use in rhizosphere carbon budget estimations. Soil Biol Biochem 26:161–170 Thierron V, Laudelout H (1996) Contribution of root respiration to total CO2 efflux from the soil of a deciduous forest. Can J For Res 26:1142–1148 Trumbore S (2006) Carbon respired by terrestrial ecosystems – recent progress and challenges. Global Change Biol 12:141–153 Trumbore S, Salazar da Costa E, Nepstad DC, Barbosa de Camargo P, Martinelli LA, Ray D, Restom T, Silver W (2006) Dynamics of fine root carbon in Amazonian tropical ecosystems and the contribution of roots to soil respiration. Global Change Biol 12:217–229 Xu M, DeBiase TA, Qi Y, Goldstein A, Liu Z (2001) Ecosystem respiration in a young ponderosa pine plantation in the Sierra Nevada Mountains, California. Tree Physiol 21:309–318
123
